Neurological gait disorders in elderly people Clinical approach and classification

Review
Neurological gait disorders in elderly people: clinical
approach and classification
Anke H Snijders, Bart P van de Warrenburg, Nir Giladi, Bastiaan R Bloem
Gait disorders are common and often devastating companions of ageing, leading to reductions in quality of life and
increased mortality. Here, we present a clinically oriented approach to neurological gait disorders in the elderly
population. We also draw attention to several exciting scientific developments in this specialty. Our first focus is on
the complex and typically multifactorial pathophysiology underlying geriatric gait disorders. An important new
insight is the recognition of gait as a complex higher order form of motor behaviour, with prominent and varied
effects of mental processes. Another relevant message is that gait disorders are not an unpreventable consequence of
ageing, but implicate the presence of underlying diseases that warrant specific diagnostic tests. We next discuss the
core clinical features of common geriatric gait disorders and review some bedside tests to assess gait and balance. We
conclude by proposing a practical three-step approach to categorise gait disorders and we present a simplified
classification system based on clinical signs and symptoms.
Introduction
Gait disorders are common in elderly populations and
their prevalence increases with age. At the age of 60 years,
85% of people have a normal gait, but at the age of
85 years or older this proportion has dropped to 18%.1,2
Gait disorders have devastating consequences. Perhaps
the most notorious corollary is falling, which is often
caused by an underlying gait problem. Injuries caused by
accidental falls range from relatively innocent bruises to
major fractures or head trauma. Another important
consequence is reduced mobility, which leads to loss of
independence. This immobility is often compounded by
a fear of falling, which further immobilises patients and
affects their quality of life.3 Importantly, gait disturbances
are also a marker for future development of cardiovascular
disease and dementia.4–6 These associations suggest that
gait disturbances—even when they present in isolation—
can reflect an early, preclinical, underlying cerebrovascular
or neurodegenerative disease. Finally, gait disorders are
associated with reduced survival, which can be attributed
to a combination of fatal falls, reduced cardiovascular
fitness, and death from underlying disease.7–9
Elderly patients regularly present with complex gait
disorders, with concurrent contributions from multiple
causal factors.10 To describe specific gait disorders
accurately is often difficult. Here, we provide a practical
approach that may support clinicians in their everyday
management of neurological gait disorders in elderly
people. We briefly address the pathophysiology of gait
disorders and discuss the effects of mental function and
normal ageing on gait. We conclude by describing a
practical clinical approach and simplified classification
system to differentiate gait disorders in everyday practice,
based on clinically discernable gait patterns. Treatments
for geriatric gait disorders are not reviewed.
Pathophysiology of gait disorders
Normal gait requires a delicate balance between various
interacting neuronal systems (figure 1) and consists of
three primary components: locomotion, including
http://neurology.thelancet.com Vol 6 January 2007
initiation and maintenance of rhythmic stepping;
balance; and ability to adapt to the environment.
Dysfunction in any of these systems can disturb gait.
Most ambulatory problems in elderly people are caused
by concurrent dysfunction of multiple systems.
Virtually all levels of the nervous system are needed for
normal gait.11–14 Recent studies have drawn attention to
pattern generators in the spinal cord that generate
rhythmic stepping.15 Neuroimaging studies point to the
role of the frontal cortex in controlling gait and in
coordinating automatic and voluntary movements.16 One
interesting study used functional MRI to identify patterns
of brain activity while participants imagined standing,
walking, or running while lying in the scanner.17 With
running (automated locomotion), spinal pattern
generators and the cerebellum were involved, whereas
slow walking evoked activity in the parahippocampal
region, presumably because spatial navigation becomes
more important.
Lancet Neurol 2007; 6: 63–74
Department of Neurology and
Parkinson Center Nijmegen,
Radboud University Nijmegen
Medical Centre, Nijmegen,
Netherlands (A H Snijders MD,
B P van de Warrenburg MD,
B R Bloem MD); and Movement
Disorders Unit, Parkinson
Center, Department of
Neurology, Tel-Aviv Sourasky
Medical Center, Sackler School
of Medicine, Tel-Aviv
University, Tel-Aviv, Israel
(N Giladi MD)
Correspondence to:
Dr Bastiaan R Bloem, Medical
Director, Parkinson Center
Nijmegen (ParC), Department of
Neurology, Radboud University
Nijmegen Medical Centre,
PO Box 9101, 6500 HB
Nijmegen, Netherlands
[email protected]
Gait and mental function
Walking is traditionally seen as an automatic motor task
that requires little, if any, higher mental functions. In the
past decade, new insights have drawn attention to the
importance of cognition in daily walking.18 Normal
walking requires strategic planning of the best route, as
well as continuous interaction with the environment and
with internal factors. Failing to understand the significance
of an obstacle, choosing an inappropriate route, or
misinterpreting one’s own physical abilities can all lead to
falls. The safety and efficacy of normal walking rely not
only on sensorimotor systems, but also critically depend
on the interaction between the executive control
dimension (integration and decision of action) with the
cognitive dimension (eg, navigation, visuospatial
perception, or attention) and the affective dimension
(mood, cautiousness, and risk-taking). A common situation where such an integration is challenged is when
people must walk while performing one or more
secondary tasks. Lundin-Olsson and colleagues19 were
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Review
Feedback:
Vestibular system
Visual system
Sensory nerves
Support:
Cardiovascular system
Bones
Joints
Ligaments
Feet
Execution:
Frontal cortex
planning
Basal ganglia
initiation, automatisation
Brainstem
integration
Cerebellum
coordination, adaptation
Spinal cord
spinal pattern generators
Nerve roots
Peripheral nerves
(both motor and sensory)
Muscles
circumstances, young healthy people begin to neglect the
secondary task and lend more priority to walking safely.
This prudent posture-first strategy is diminished in
elderly people,20 and failure to prioritise gait under
difficult circumstances is weakly associated with falls.25
Research has shown that frontal executive functions
are especially important for maintaining walking stability.
Dysexecutive functions can be the primary cause of falls
in a group of idiopathic elderly fallers.26,27 The involvement
of cognitive control in normal gait could explain why falls
are so common in patients with dementia and why
demented patients are so vulnerable to dual task
performance while walking.28,29 Interestingly, patients
with Parkinson’s disease whose phenotype is dominated
by postural instability and gait disorder have a much
greater risk of cognitive decline and dementia than do
patients with tremor-dominant Parkinson’s disease.30,31
Additionally, adverse effects on cognitive gait control
might explain the high incidence of falls and injuries in
individuals taking psychoactive medication.32
Affective disorders are also associated with gait
problems in elderly people. For example, depression,
anxiety, and particularly fear of falling are common
consequences of unsecured gait and falls among elderly
people.33–35
In view of these complex interactions between walking,
cognition, and mood, new interventional strategies
should be developed to promote secured mobility of
elderly people by improving attention, dual task
performance, mood, and executive functions.36
Effect of normal ageing on locomotion and gait
Figure 1: Levels of the central and peripheral nervous system required for normal gait
the first to note the significance of a failure to maintain
a conversation while walking (“stop walking while
talking”) as a marker for future falls. The ability to
maintain normal walking while performing a secondary
task (dual task paradigm) has become the classic way to
assess the interaction between cognition and gait.20 In
elderly people, this dual task ability deteriorates because
central resources decline, secondary to subclinical disease
processes or medication. This deterioration leads to a
mismatch between the limited personal resources of
elderly people and the complexity of the demand (the
combined walking and secondary task). As a consequence,
elderly people slow down or have an increased stride
variability (suggesting reduced automaticity) while performing a secondary task during walking.21 Gait becomes
less secure and the risk of falling increases. In patients
with overt disease, such as stroke or Parkinson’s disease,
gait deteriorates even more during dual tasking.22–24
Another form of dual task impairment is when elderly
people fail to get their priorities right.25 Under complex
64
Ageing is typically equated with abnormalities, and this
association certainly applies to gait. Many older people
accept their gait difficulty as being normal for their age
and their doctors often support them in this view. But
are gait disorders truly an inevitable consequence of
ageing itself? This question is illustrated by the evolving
concepts around the so-called senile gait disorder: the
slow, shuffling, and cautious walking pattern commonly
seen in older age. Because clinical examination reveals
no apparent cause, normal ageing was long held
responsible for this disorder. However, recent findings
have challenged this concept. Up to 20% of very old
individuals walk normally, hence gait disorders are
certainly not an inevitable feature of old age.1 This
finding indirectly implies that those who have
gait impairment in fact suffer from underlying disease.
This assumption is lent support by the fact that
individuals with a senile gait disorder have an increased
risk of becoming demented5 and have reduced survival
compared with age-matched individuals who walk
normally at a high age (figure 2).4 These findings
suggest that senile gait disorders are an early
manifestation of underlying pathology, most notably
subtle white-matter changes, vestibular dysfunction,
visual changes, or oculomotor changes.37–43 Such
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Review
Differentiation of gait disorders
Only few studies describe the distribution of geriatric
gait disorders. Obviously, the spectrum of underlying
illnesses will depend on the population under
consideration and the assessment technique. Within a
relatively healthy subgroup of 153 community residents
aged 88 years and older, about 61% reported distinct
diseases as a cause of gait impairment.1 Non-neurological
disorders were the leading causes of gait impairment, in
particular joint pain (52 of 87 people), whereas many
others had multiple causes for their gait impairment.
Stroke was the most common neurological cause. In
another study of 120 elderly outpatients seen in a
neurological reference practice, the most common causes
for gait disorders were sensory ataxia (18%), myelopathy
(17%), multiple strokes (15%), and parkinsonism (12%).2
Largely the same causes dominated in a series of 493
neurological inpatients, 60% of whom had a gait
disorder.44
Recognition of specific gait disorders
Table 1 summarises the main features of the weak,
spastic, and ataxic gait disorders (for reviews, see
references 13,15,45,46). Because these categories usually cause
little difficulty in clinical practice, we focus next on the
remaining gait disorders.
1·0
0·8
Cumulative survival
disorders might alter gait directly, but may also act in
an indirect way by causing a subjective sensation of
instability and insecurity, forcing individuals to
purposely adopt a more cautious gait.
The message for clinicians is that gait disorders in
elderly people are not merely the unpreventable
consequence of ageing. Instead, these gait disturbances
more likely result from the increased prevalence and
severity of (clinical or subclinical) diseases with increasing
age (figure 3). For this reason, we suggest abandoning
the term senile gait as a specific gait category.
0·6
0·4
Normal gait
Senile gait disorder
Gait disorder due to disease
0·2
0·0
0
1
2
3
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6
Figure 2: Kaplan-Meier curves showing cumulative survival due to all causes of death
Results are shown for patients with a completely normal gait (n=25), those with senile gait disorders (n=14), and
those with gait disorders due to known disease (n=87). Mean age was 90 years in all groups (range 87–97 years).
Survival was different between the groups (log-rank p=0·01). All-cause-mortality risk was increased in people with
senile gait disorders compared with those with a normal gait (RR=2·8; 95% CI 1·1–7·3, p = 0·03) and was similar to
those with gait disorders due to known disease (RR=1·2; 95% CI 0·6–2·5, p=0·6). Mortality due to cardiovascular
disease also differed among the three groups, with a two-fold increased risk of cardiovascular death in people with
senile gait disorders compared with those with normal gait (data not shown). Reproduced with permission from
Blackwell Publishing.4
Gait disorders
Falls
Mortality
Injuries
Age-related
pathology
?
Fear of
falling
Hypokinetic-rigid gait disorders
Diseases of the basal ganglia and the frontal lobe mostly
present with a hypokinetic-rigid gait. However, frontal
pathology can also cause a higher level gait disorder in
which truncal imbalance and frequent falls are a key
feature. Other associated features of this higher level gait
disorder are depression, frontal release signs, and
impaired executive function.47 Specific features of gait,
posture, or balance can assist in the differential diagnosis
of these different disorders (table 2). A characteristic
feature of hypokinetic-rigid gait is shuffling with a
reduced step height, often with a reduced stride length,
leading to slowness of gait. The base of support is typically
normal in Parkinson’s disease, but is often widened in
patients with atypical parkinsonism. Other characteristic
features include reduced arm swing (asymmetrical in
Parkinson’s disease, but more symmetrical in atypical
parkinsonism), which can present in isolation and
4
Survival (years)
Ageing
Immobility
Morbidity
(cardiovascular disease,
cognitive decline)
Reduced quality
of life
Figure 3: Indirect association between ageing and geriatric gait disorders
This association occurs mainly, if not exclusively, via the intermediate of age-related pathology. Adverse
consequences of gait disorders in elderly people include reduced quality of life and, eventually, reduced survival.
precede the onset of other hypokinetic-rigid features by
many years. Turning movements become slow and are
executed en bloc. Festination is a feature of more
advanced disease, where patients take rapid small steps
in an attempt to maintain the feet beneath the forward
moving trunk. Poorly mobile patients with advanced
disease can sometimes respond quickly to environmental
events—typically emotional or threatening circumstances—and move unexpectedly well (kinesia paradoxica). Apparently, patients with Parkinson’s disease
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Elements of the clinically based diagnostic work-up
Main features of gait
Antalgic gait
Reduced stance phase on affected limb
Limping
Paretic/hypotonic gait
High steppage
Dropping foot
Waddling
Spastic gait
Circumduction
Intermittent abduction of ipsilateral arm with each step
Foot dragging: audible “scuffing toe”
Scissoring; bilateral circumduction
Vestibular gait
Deviation to one side
Specific gait or balance test*
Associated symptoms and signs
Pain
Limited range of movements
Trendelenburg’s sign
Lower motor neuron features (eg, weakness,
atrophy, low to absent tendon reflexes)†
Pyramidal syndrome
Anterior-medial side of the shoe sole worn out
Aggravated by eye closure
Positive Unterberger test
Vestibular features (eg, nystagmus, abnormal
tilting test)
Sensory ataxic gait
Staggering, wide based
Aggravated by eye closure
Disturbed proprioception
Cerebellar ataxic gait
Staggering, wide based
Not aggravated by eye closure
Cerebellar ataxia (eg, dysarthria, hypermetria,
nystagmus)
Dyskinetic gait
Extra movements that affect gait
Can be task-specific (eg, dystonic gait)
Features of dystonia, chorea, myoclonus or tics
Hypokinetic-rigid gait
Shuffling (slow speed, short stride, rigidity, reduced step height) Improves with external cues
Hesitation and freezing
Aggravation by secondary task
Hypokinetic-rigid features (eg, bradykinesia,
resting tremor)
Cautious gait
“Walking on ice”; slow, wide base, short steps
Striking improvement with external support
Postural instability (mild to moderate)
Excessive fear of falling
Higher level gait disorder
Severe balance impairment (no rescue reactions with the
pull test; “falling like a log”)
Inadequate synergies
Inappropriate or bizarre foot placement
Crossing of the legs
Leaning into wrong direction when turning or standing
Variable performance (influenced by environment
and emotion)
Hesitation and freezing (ignition failure)
Abnormal interaction with environment (eg, trouble
adapting with walking aids; no benefit from cues)
Sometimes better able to perform cycling leg
movements while recumbent (gait “apraxia”)
Frontal release signs
Executive dysfunction
Depression
Frequent falls
A clinically based diagnosis for each gait syndrome can usually be reached with a systematic approach: first, a description of the core gait features; next, the use of specific gait or balance tests; and finally, a search
for associated symptoms and signs. *Simple diagnostic tests that can be done at the bedside include: providing external support (eg, a walking aid); imposing secondary tasks while walking (dual or multiple
tasking); eye closure; walking backwards; influence of external cues (visual; auditory; or mental). †Peripheral neuropathy and radiculopathy are among the most common causes of gait difficulties in the elderly.
Table 1: Main features of specific gait syndromes
can use such external triggers to engage alternative motor
circuits and thereby bypass the defective basal ganglia
circuitry.48
Hypokinetic-rigid gait disorders can be classified
according to the underlying anatomical substrate. One
main group involves lesions within the basal ganglia and
their connections to the frontal cortex, brainstem, or
both. Pathological changes in the frontal lobe itself can
also contribute to a hypokinetic-rigid gait. There are no
well-defined clinical markers for frontal-lobe contribution,
but suggestive features include a wide-based or variable
stance and truncal imbalance. Some would also include
gait apraxia here, often defined as a marked discrepancy
between the severity of the gait disorder and the ability to
perform other leg movements, such as cycling in the air
while lying down. Associated features include urinary
urgency and cognitive changes and a poor response to
external cues.
Hypokinetic-rigid gait disorders can also be classified
according to the underlying disease process. One
important group includes neurodegenerative disorders
such as Parkinson’s disease and various forms of atypical
parkinsonism (eg, multiple system atrophy or progressive
supranuclear palsy). Another common group includes
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underlying cerebrovascular disease. Gait disorders with a
mixed hypokinetic-rigid and ataxic character are a
common occurrence in patients with subcortical
arteriosclerotic encephalopathy.49 A less common feature
of cerebrovascular disease is lower body parkinsonism, a
predominance of symptoms and signs in the legs, with a
relatively preserved arm swing and little bradykinesia of
the hands.50,51 The term lower body parkinsonism is a
useful descriptive term in clinical practice because it
refers to a recognisable phenotype that is often associated
with underlying cerebrovascular disease, including whitematter changes and lacunar infarcts in the basal ganglia.
However, lower-body parkinsonism is not synonymous
with vascular parkinsonism. Occasional patients can
present with a clinical presentation resembling
Parkinson’s disease (with upper-limb involvement) or
even progressive supranuclear palsy. Hypokinetic-rigid
gait disorders due to cerebrovascular disease can develop
acutely or with an insidious onset.50 The acute syndrome
mainly involves infarcts in the putamen, globus pallidus,
or thalamus, whereas the gradual form is associated with
diffuse white-matter changes.
A third type of underlying disease process is ventricular
widening, as occurs in patients with normal pressure
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Main anatomical substrate
Disease process
Characteristic features
Associated features
Parkinson’s disease (PD)
Substantia nigra
Neurodegenerative
Narrow-based gait
Asymmetrical presentation
Stooped posture
Early freezing and falls rare
Good response to
levodopa
Resting tremor hand(s)
Multiple system atrophy,
parkinsonian type
Basal ganglia
Cerebellum
Pyramidal tracts
Autonomic nervous system
Neurodegenerative
Early phase like PD gait
Later phase more wide-based
Pisa syndrome
Antecollis
Vertical falls (due to syncope)
Cerebellar ataxia
Autonomic features
Pyramidal signs
Progressive supranuclear
palsy
Diffuse brainstem pathology
Neurodegenerative
Wide-based gait
Freezing common
Erect posture, but with retrocollis
Early/spontaneous/backward falls
Motor recklessness
Frequent and severe injuries
Vertical gaze palsy
Pseudobulbar palsy
Frontal dementia
Applause sign
Corticobasal degeneration
Basal ganglia
Cortex
Neurodegenerative
Asymmetrical presentation—eg, unilateral
leg apraxia, dystonia, or myoclonus
Later: wide-based gait, freezing, shuffling
Apraxia
Alien limb
Cortical sensory loss
Dementia with Lewy bodies
Basal ganglia
Cortex
Neurodegenerative
Like PD gait
More symmetric
Dementia
Fluctuations
Visual hallucinations
Subcortical arteriosclerotic
encephalopathy
Subcortical white matter
Vascular
Small steps
Wide-based gait
Start hesitation
Variable timing and amplitude of steps
Urinary incontinence
Cognitive decline
Stepwise progression
Vascular parkinsonism
Diffuse white matter
Basal ganglia
Vascular
Lower body parkinsonism
More wide based
Less stooped
Relatively preserved arm swing
Urinary incontinence
Cognitive decline
Stepwise progression
Strategic vascular lesion
Putamen
Globus pallidus
Thalamus
Dorsal mesencephalon
Vascular
Lower body parkinsonism
Freezing/severe gait akinesia
Severe disequilibrium
Drifting to one side
Normal pressure
hydrocephalus
Frontostriatal (periventricular) Ventricular widening Wide-based gait, freezing, gait apraxia
Truncal imbalance
Preserved arm swing
Drug-induced parkinsonism Basal ganglia (postsynaptic)
Mild gait impairment, rarely freezing
Preserved postural reflexes
Pisa syndrome
Urinary incontinence
Cognitive decline
Upper limb tremor
Symmetrical presentation
Table 2: Differential diagnosis of parkinsonian disorders, based on specific features of gait, balance, or posture
hydrocephalus. Whether normal pressure hydrocephalus
truly exists as a separate entity with its own unique
pathophysiology is unknown. Typically, the disorder
presents with a recognisable triad of hypokinetic-rigid
gait impairment, urinary incontinence, and (frontal)
dementia. Gait is characterised by marked slowing and
small shuffling steps and regular freezing, but usually
with largely preserved arm movements.52,53 Ataxic
elements are also seen, including a broad stance width
and an increased variability in timing and amplitude of
the steps. The pathophysiology has not been clarified,
but may relate to an excessive volume of intraventricular
cerebrospinal fluid that is not explained by cerebral
atrophy. The classic radiological appearance includes
widened lateral ventricles (especially affecting the
anterior horns), often accompanied by periventricular
white-matter lesions. An unresolved question (yet one
with direct implications for treatment) is whether these
periventricular white-matter lesions are the cause or
consequence of ventricular widening.54
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Clinical examination alone cannot always disentangle
these different anatomical and pathophysiological causes
of hypokinetic-rigid gait disorders, especially in early
stages where overlap is substantial. In such patients, it is
best to refrain from confusing terminology. It initially
suffices to classify the patient as having a hypokineticrigid gait disorder and to base a more definitive
anatomical or aetiological diagnosis on ancillary
investigations (MRI) and sometimes the response to
treatment (eg, a trial of levodopa).
Cautious and careless gaits
Typically, people with a cautious gait move slowly, with a
wide base and short strides, with little movement of the
trunk, while the knees and elbows are bent. Cautious gait
is common in elderly people and originates in part from
fear of falling, which is sometimes present to the degree of
panic.33 There are two main subgroups. In the first, fear of
falling is excessive relative to the degree of actual instability.
In fact, balance can be fully normal, as in people with a
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pathological fear of falling (fall phobia) caused by a single
fall. In these individuals, the remaining neurological
examination is completely normal, and provision of
external support or reassurance can substantially improve
gait. In the second subgroup, fear of falling is justified by a
recent history of recurrent falls or by a self-perceived
instability due to overt or sometimes otherwise subclinical
underlying disease. These individuals might show mild
freezing of gait, occurring mainly with gait initiation and
while turning.33 Neurological examination can further
reveal mild hypokinetic-rigid signs, disturbed postural
responses, and frontal release signs. With time, these
patients may develop other subcortical or frontal
disturbances, or progress to having a more disabling gait
impairment. A therapeutic levodopa trial is justifiable, but
it has been our clinical impression that after a short positive
response that could represent a placebo effect, patients
with cautious gait no longer improve. Fear has to be treated
medically or behaviourally.
Careless gait is the counterpart of the cautious gait.
Some patients seem overly confident and walk
inappropriately fast, perhaps because of lack of insight or
frontal-lobe disinhibition. Notorious examples are
patients with progressive supranuclear palsy and
Huntington’s disease who typically move too abruptly
despite a severe balance deficit and who seem unable to
properly judge the risk of their actions. This motor
recklessness probably underlies the high incidence of
fall-related injuries in these disorders.55,56 A similar
recklessness contributes to falls and injuries in ageing
disorders such as Alzheimer’s disease. Confusion and
delirium can also contribute to a careless gait. A recent
study showed that gait velocity should be judged in the
context of the patient’s physical capabilities. Thus,
although frail elderly patients with dementia walked
slowly, they still walked relatively too fast, given their
overall degree of physical impairment, which should
have warranted an even much slower gait.57 For some
cognitively impaired patients, restriction of unsupervised
physical activities is an ultimate measure to prevent
wandering behaviour and to reduce injurious falls.58
Fluctuating or episodic gait disorders
A curious feature of some gait disturbances is their
fluctuating or frank episodic nature. The specific
provoking factor can differentiate these gait disturbances.
Some gait disorders fluctuate more or less predictably
because of exercise intolerance or pain. In elderly people,
walking difficulties after exercise are often due to fatigue
(cardiopulmonary or neuromuscular disease), but might
also indicate vascular or neurogenic claudication.
Psychogenic gait disorders can also present with an
episodic character, for example an aggravation when
bystanders are present.
Other gait disorders are truly episodic. The sudden and
largely unpredictable nature of these episodes is
incapacitating, commonly leading to falls because
68
patients are caught unprepared.59 An example is freezing
of gait, where patients suddenly experience a characteristic
feeling “as if the feet become glued to the floor”. Various
terms have been used in different contexts, including
gait ignition failure or slipping clutch phenomenon. We
propose to use the term freezing of gait to describe all
gait initiation disturbances. Although freezing of gait is
most often observed when initiating gait, it also occurs
when walking through a narrow passage, during turning,
while executing a secondary task (eg, responding to a
question), or upon reaching a destination. In severely
affected patients, it can occur seemingly spontaneously
while walking in open terrain. Three different clinical
presentations are recognised: shuffling with small steps;
trembling in place, while attempting to overcome the
block; or being fully unable to start or continue walking,
which is relatively rare.59 Freezing of gait can present
largely in isolation, as occurs in primary progressive
freezing gait. This usually results from frontal lobe
damage, irrespective of the specific disease process.49
However, freezing of gait is mostly seen as part of a
hypokinetic-rigid syndrome, including Parkinson’s
disease and various forms of atypical parkinsonism.60,61
Dyskinetic gait disorders
The term dyskinesias includes all involuntary movements
or postures—eg, chorea or dystonia. Presence of such
involuntary movements during walking suggests a
dyskinetic gait. A well-known example is the gait in
patients with postanoxic encephalopathy, in which the
positive and negative action myoclonus (Lance-Adams
syndrome) produces a bouncing gait and stance.
Dyskinesias can contribute to falls by causing excessive
trunk movements beyond the limits of stability, as occurs
in patients with Parkinson’s disease with medicationinduced dyskinesias62 or in patients with Huntington’s
disease.56 Note that dyskinesias might be absent during
clinical examination because of their fluctuating character
or because patients suppress them intentionally.
Cognitive distractions can help to elicit the involuntary
movements during examination.
Patients with dystonia require specific attention because
their gait or balance impairment can be task-specific. For
example, patients may have severe gait impairment due
to leg dystonia, but can easily walk backwards or even
run. This is easily misinterpreted as a psychogenic sign.
Examples of gait dystonia include early onset Parkinson’s
disease presenting with a foot dystonia while walking, or
patients with idiopathic torsion dystonia who can present
with unusual gait patterns. Other forms of gait dystonia
include retrocollis in patients with progressive supranuclear palsy, antecollis or a Pisa syndrome (severe and
persistent lateroflexion of the trunk) in patients with
multiple system atrophy, and an asymmetrical arm or leg
dystonia during walking in patients with corticobasal
degeneration. Many dystonic patients tend to walk on
their toes (cock walk). Axial forms of dystonia, including
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dystonic scoliosis, hyperlordosis, or torticollis can also
interfere with walking and standing. This is particularly
true if extensor or flexor spasms are present.
Psychogenic gait disorders
Although suspicion of psychogenic gait disorders is
highest in younger patients, they can occur in elderly
patients. Psychogenic gait is often not compatible with
known gait patterns and they can take unusual forms
(panel).63–65 Falls and injuries are thought to be rare in
patients with a psychogenic gait, but we encountered one
such patient who sustained severe injuries (epidural
haematomas and a skull base fracture).65 Care must be
taken not to miss underlying organic disease, in particular
frontal-lobe dysfunction. The differential diagnosis
includes organic gait disorders that can mimic
psychogenic gait disturbances; examples include
choreatic gait in Huntington’s disease, task-specific
dystonic gait, episodic weakness in myasthenia gravis,
and cataplexy. Gait in stiff person syndrome can also look
strange; gait abnormalities typically aggravate when
patients are instructed to hurry up.66
Panel: Features suggestive of a psychogenic gait disturbance
Suggestive features
• Incongruous with known gait disorders
• Bizarre presentation
• Variable, inconsistent pattern
• Non-physiological pattern
• Rare falls or injuries*
• Abrupt onset
• Extreme slowness
• Unusual or uneconomic posture
• Exaggerated effort
• Sudden buckling of the knees
Associated features
• Incongruous affect (belle indifference)
• Secondary gain
• Prior history of psychiatric disease†
*Striking exemptions with sometimes severe injuries have been described.65 †Rare, but
diagnostic yield is higher with an intensive interview.
Comments
Gait disorders and falls caused by medication
Gait disorders and falls in elderly people are commonly
associated with adverse effects of drugs (table 3).32,67–76 The
precise underlying pathophysiological mechanism is
unclear in many cases. Commonly implicated factors
include sedation, orthostatic hypotension, behavioural
abnormalities, extrapyramidal side-effects, or ataxia.
However, there can also be confouding by indication—ie,
falls that are caused by the underlying disorder for which
the drugs were prescribed in the first place. Thus, falls or
a disturbed gait in patients taking anti-diabetic medication
might simply be caused by an underlying diabetic
polyneuropathy. Polypharmacy is particularly associated
with falls, but only if a patient daily takes at least one
drug with an established risk of increasing falls.77 A
critical review of medication is therefore important in
elderly people. For example, a recent randomised
controlled trial showed that when a pharmacist reduced
the number of drugs in elderly care-home residents, the
number of falls was reduced by 40%.78
Assessment of gait disorders
Assessment includes a full physical and neurological
examination and a systematic gait assessment. Use of
standard rating scales, such as the Tinetti mobility index79
or gait and balance scale,80 help to score all different
elements of gait and balance. Most examination rooms
are too small, so it is often necessary to examine the
patients while walking in the corridor. Simple undisturbed
gait can be informative, but additional abnormalities
come to light when gait is challenged. For example,
walking with eyes closed might provoke or aggravate
ataxia in patients with a sensory neuropathy, or cause a
consistent deviation to one side in patients with unilateral
http://neurology.thelancet.com Vol 6 January 2007
Antipsychotics67,68
Occurs with both typical and atypical antipsychotics
Antidepressants68,69
Occurs with both SSRIs and tricyclic antidepressants
Anticonvulsants68,70
Occurs with both older anti-epileptic drugs (eg, phenobarbital) and newer
anti-epileptic drugs (eg, lamotrigine), but possibly less with the newer drugs
Antiparkinson drugs71
Occurs with all classes of antiparkinson drugs. Underlying mechanism is complex,
but mainly includes excessive dyskinesias, orthostatic hypotension, and
behavioural abnormalities
Benzodiazepines/
other hypnotics68,72
Occurs with both short and long-acting benzodiazepines. Newer ‘Z’-compound
hypnotics such as zopiclone are thought to be safer
Analgesics68,73,74
Occurs with opiates, NSAIDs, and paracetamol. Some studies find stronger effects
of opiates, others of NSAIDs
Antihypertensive74
Diuretics, beta-blockers, ACE inhibitors, and nitrates
Evidence is stronger for inpatients than for outpatients, probably due to a stronger
effect of orthostatic hypotension after prolonged bed-rest
Anticholinergics68,75
Both sedation and orthostatic hypotension may contribute
Antidiabetics76
Perhaps via underlying pathology—eg, diabetic polyneuropathy or cerebrovascular
disease
Anti-arrhythmics74
..
Quinine68
Quinine and derivates
SSRIs=selective serotonin reuptake inhibitors. NSAID=non-steroidal anti-inflammatory drug. ACE=angiotensinconverting enzyme.
Table 3: Drugs with adverse effects on gait, posture, and balance
vestibular loss. Patients suspected of having freezing of
gait often walk normally in the examination room because
excitement associated with the doctor’s visit can suppress
this sign. In such patients, careful questioning supported
by validated questionnaires81 is important. Additionally,
walking in tight quarters, while turning or when doing
secondary tasks may provoke freezing of gait.
Next to challenging gait, observation of whether
patients can improve their gait—eg, by benefiting from
walking aids or provision of external support—is equally
instructive. Seemingly incapacitated patients with a
69
Review
cautious gait can show striking improvements in gait
when provided with external support while walking.
Similarly, providing individuals with external visual,
auditory, or mental cues can help to reduce freezing of
gait.36 By contrast, patients with a higher-level gait
disorder typically do not benefit from external cues and
have troubles adapting with walking aids. Such patients
are sometimes better able to perform cycling leg
movements while lying recumbent, suggesting that their
loss of control over leg movements is task-specific (gait
apraxia). As mentioned earlier, this task-specificity can
also be seen in patients with dystonia.
The pull test (or retropulsion test) is commonly used to
probe the reactive and defensive balance reactions.82,83
Many variants exist, but most commonly the investigator,
standing behind the patient, suddenly pulls the patient’s
shoulders. The test is typically used to score the severity
of postural instability. However, failure to initiate a
corrective step—due to freezing of gait—also produces
an abnormal test result. We usually deliver one shoulder
pull without specific prior warning, as this best mimics
daily life circumstances where falls are usually unexpected
events. We then repeat the test several times and regard
failure to habituate to the test as another sign of balance
impairment. A recently introduced variant is the push
and release test, which rates the postural response to a
sudden release of a patient pressing backward on an
examiner’s hands placed on the subject’s back. An
advantage is that this test allows examiners to apply more
consistent perturbation forces to the patients than with
the conventional pull test, and the outcome seems to
correlate better with self-reported falls.84
Timed tests can be used to quantify gait velocity (eg, to
assess the effect of treatment), but these do not
accommodate the quality of gait. A commonly used test is
the timed up and go test, where patients are observed and
timed while rising from a high chair with arms, walking
3 m, turning around, walking back, and sitting down
again.85 Cognition and affect should be routinely examined
in elderly patients with gait problems, with emphasis on
frontal cognitive dysfunction. Fear of falling can be
assessed directly or, preferably, by using a validated
questionnaire.3 Finally, it is important to assess footwear
and vision (with and without correction), as these
contribute to gait disorders and falls in the elderly.86,87
A relatively new method is physiological analysis of gait,
by use of a treadmill and quantitative outcome measures:
kinematics (joint motion), kinetics (reactive forces), and
dynamic electromyography. An important disadvantage is
that gait is assessed under constrained and highly
unnatural circumstances, leading to lack of ecological
validity.88 Less complex systems can be applied in freely
moving individuals. Common tools are ambulatory
goniometers or accelerometers, to quantify movement of
the limbs or trunk,89 and shoes with pressure-sensitive
insoles90,91 or a carpet with pressure-sensitive sensors92 to
measure subtle changes in locomotion rhythmicity,
variability, or left–right synchronisation. Although this
type of gait analysis better approaches real-life situations,
whether the currently available equipment provides any
clinically relevant extra information is unknown. We
therefore feel that it is currently not worth sending elderly
patients for a quantitative study of gait in a sophisticated
gait laboratory. Possible exceptions include a preoperative
assessment to guide the surgeon before an orthopaedic
intervention, detailed electromyography studies in spastic
or dystonic patients to fine-tune subsequent treatments
with botulinum toxin or selective surgical denervation,
and kinematic gait analyses to assist rehabilitation
specialists in their choice for specific segmental orthoses
or adjusted footwear.93–97 Physiological gait analysis is a
very useful technique for scientific purposes.
Clinical approach and classification of gait
disorders
We conclude our contribution by discussing a new,
practically oriented approach to gait disorders, as well as
a simplified modification of the classification originally
proposed by Nutt and colleagues.98 A broadly accepted
classification system would assist health professionals
when they communicate about patients with gait
disorders. Research will also benefit from a good
classification system, for example to ascertain that
properly diagnosed patients and homogeneous groups
are included in trials or gait experiments.
Different types of gait classifications currently exist,
with different and partly overlapping starting points
(hierarchical, anatomical, aetiological, or phenomenological). Every classification system has inconsistencies (table 4). We propose a practical three-step
Examples
Drawbacks
Hierarchical
Lower level
Intermediate level
Higher level
Term higher level often abused as basket term for any poorly understood gait disorders
Subdivisions of higher level gait disorders difficult to use in clinical practice
Overlap in symptoms between middle and higher level gait disorders
Anatomical
Frontal gait
Cerebellar gait
Different anatomical lesions may present with similar gait patterns
Any given anatomical lesion may present with different gait patterns
Aetiological
Vascular
Neurodegenerative
Ancillary studies or post-mortem examination often required to make definitive diagnosis
Phenomenological
See table 1
Pathophysiology not taken into account
Table 4: Drawbacks of currently available gait classification systems
70
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http://neurology.thelancet.com Vol 6 January 2007
Specific gait or balance tests
Associated symptoms and signs
Step 1
Core gait features
Possible gait disorder (clinically based gait syndrome)
Therapeutic investigations
Disease progression
Step 2
Ancillary investigations
Probable gait disorder
Post-mortem examination
Step 3
approach that begins with a gait classification based on
clinical phenomenology, as observed in the consultation
room (step 1 in figure 4). This first step includes three
elements: the core features of a patient’s gait; additional
clinically based gait and balance tests; and associated
neurological or physical abnormalities. These three
elements are all listed systematically in table 1 for each of
the main clinically discernable gait patterns. For example,
patients with an ataxic gait typically have a wide-based,
staggering gait (core clinical feature). By itself, this core
feature can implicate either sensory ataxia or cerebellar
ataxia, and this distinction can be made with additional
gait and balance tests, such as the effect of eye closure
(aggravates the gait impairment much more in sensory
ataxia compared with cerebellar ataxia). The distinction
between both types of ataxic gait disorders can be
corroborated by a search for associated neurological or
physical abnormalities: hypermetria, nystagmus, and
cerebellar dysarthria suggest that the wide-based gait was
in fact caused by cerebellar ataxia, whereas disturbed
proprioception would suggest sensory ataxia. Taken
together, the three elements of this first step thus lead to
a clinically based classification, determined by
recognisable gait features (syndromes or possible gait
disorders), as listed in the left column of table 1.
Note that this first step of the classification avoids
anatomical,
pathophysiological,
and
aetiological
terminology because it is solely based on clinical
impressions obtained in the examination room. For that
reason, our clinical classification also avoids a distinct
categorisation of low level and middle level gait disorders
as proposed in the original Nutt classification98 because
this hierarchical distinction formally requires ancillary
studies to demonstrate the site of the lesion. Also,
symptoms can overlap between middle level and higher
level gait disorders.
We propose to abandon the anatomically based term
frontal gait disorders, as these may present with at least
three different phenotypes: a shuffling hypokinetic-rigid
gait; a wide-based ataxic pattern; and an episodic gait
disorder, dominated by freezing episodes. Furthermore,
the frontal phenotype can be seen in a wide variety of
disorders, including Parkinson’s disease, various forms
of atypical parkinsonism, or frontal mass lesions.
How can we classify the gait disorders collectively
grouped under the original term higher level gait
disorders? These cannot be captured by a single,
dominant, and consistently present gait feature, but do
share a recognisable phenotype47,99 that can be identified
using the first step of our approach (table 1). We propose
to maintain the original term higher level gait disorders
until better insights arrive from pathophysiology. There
is a growing consensus to avoid, for the time being, any
further subdivisions of the higher level gait disorders, as
these have little value in clinical practice.100
A more certain clinical diagnosis (which we would define
as a probable gait disorder) often requires an additional
Definite (aetiology-based) gait disorder
Figure 4: Practical three-step approach for the classification of geriatric gait disorders
The first level yields a temporary, clinically based diagnosis, according to phenotype (possible gait disorder).
Further refinement of the diagnosis can be based on tailored ancillary studies (eg, structural neuroimaging, nuclear
imaging, or genetics), the response to treatment (eg, response to levodopa, or the effect of stopping sedative
drugs), and the factor time (disease course). This second level yields a probable gait disorder. A definite aetiological
diagnosis will often depend on post-mortem examination.
diagnostic step (step 2 in figure 4). This second diagnostic
step again involves three elements. First, for some patients,
the clinical diagnosis will serve as a guide for tailored
ancillary investigations, such as structural neuroimaging
to detect, for example, underlying cerebrovascular disease.
Second, the response to treatment will further assist in
making a definitive diagnosis. For example, a substantial
improvement of a shuffling gait disorder with levodopa
suggests involvement of a presynaptic dopaminergic
lesion, possibly due to Parkinson’s disease. Third, the
factor time may provide additional clues about the disease
course, or reveal newly emerging neurological abnormalities. For example, prolonged follow-up (up to 16 years) of
patients with a cryptogenic primary progressive freezing
gait showed a progression to recognisable clinical
diagnoses, including pallidonigroluysian degeneration,
diffuse Lewy body disease, progressive supranuclear palsy,
and corticobasal degeneration.101
The third and final step of our diagnostic approach will
lead to a definitive, aetiology-based diagnosis (step 3 in
figure 4). This step often depends on post-mortem
examination. Further enhancement of our understanding
of particular gait disorders by increasing the number of
clinicopathological correlations will be a major challenge.
Our classification does not include gait disorders that
are secondary to a clear and overriding balance problem.
71
Review
Search strategy and selection criteria
References for this review were identified by searches of
PubMed up to August 2006. Papers were also identified from
the authors’ own files and from references given in relevant
articles. Search terms “gait”, “gait disorder”, “locomotion”,
“elderly”, “geriatric”, and “ageing” were used.
5
6
7
8
We feel that these should be classified as primary balance
disorders and managed as such. An example is the
astasia-abasia syndrome due to thalamic stroke, where
gait is severely hampered not due to a defect in the neural
machinery that is responsible for maintaining gait, but to
a severe balance deficit.102
10
11
12
Conclusions
13
This review shows that the field of gait disorders is very
much on the move, with exciting new insights in the
underlying pathophysiology. There is an increasing
awareness that gait disorders in old people are often not
due to merely ageing, but rather are associated with
diseases that are more common in elderly people and
which are potentially amenable to therapeutic intervention.
Clinical assessment of geriatric gait disorders may seem
difficult, but is facilitated by the practical approach
proposed here. Modern neuroscience methods such as
functional MRI and virtual reality are now increasingly
engaged in gait research, and there is good reason to
believe that this will enhance our fundamental understanding of geriatric gait disorders, thereby opening new
avenues to improve the management of this common and
disabling problem.
14
Contributors
All authors participated in the drafting of the paper and have seen and
approved the final version. AHS did the systematic literature search,
wrote the first draft of the paper, and assisted in drafting later revisions
of the paper. BPW critically reviewed and rewrote early drafts of this
review paper and contributed to the proposed new classification system.
BRB and NG jointly formulated the outlines of this review paper,
contributed to the proposed new classification system, wrote parts of
the manuscript, and contributed to the editing process. BRB had overall
supervision of writing this review paper.
Conflicts of interest
We have no conflicts of interest.
Acknowledgments
AHS and BRB were supported by a research grant of the Princess
Beatrix Funds. NG is supported by grants from the Parkinson Disease
Association and the National Parkinson Foundation, USA.
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